Relationships between Free-Living Amoeba and their Intracellular Bacteria

Rubeniņa, Ilze; Kirjušina, Muza; Bērziņš, Aivars; Valciņa, Olga; Jahundoviča, Inese

doi:10.1515/prolas-2017-0044

Cited by 7 publications

(8 citation statements)

References 66 publications

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“…After invasion, bacteria can be retained in an environmentally resistant cyst or spore [20]. A number of bacterial pathogens, such as Legionellae pneumophila and others [21, 22], are harbored in different species of amoebae and there is a growing list of recently identified amoebae symbionts [23, 24].…”

Section: Introductionmentioning

confidence: 99%

Intracellular Burkholderia Symbionts induce extracellular secondary infections; driving diverse host outcomes that vary by genotype and environment

et al. 2019

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Symbiotic associations impact and are impacted by their surrounding ecosystem. The association between Burkholderia bacteria and the soil amoeba Dictyostelium discoideum is a tractable model to unravel the biology underlying symbiont-endowed phenotypes and their impacts. Several Burkholderia species stably associate with D. discoideum and typically reduce host fitness in food-rich environments while increasing fitness in food-scarce environments. Burkholderia symbionts are themselves inedible to their hosts but induce co-infections with secondary bacteria that can serve as a food source. Thus, Burkholderia hosts are “farmers” that carry food bacteria to new environments, providing a benefit when food is scarce. We examined the ability of specific Burkholderia genotypes to induce secondary co-infections and assessed host fitness under a range of co-infection conditions and environmental contexts. Although all Burkholderia symbionts intracellularly infected Dictyostelium, we found that co-infections are predominantly extracellular, suggesting that farming benefits are derived from extracellular infection of host structures. Furthermore, levels of secondary infection are linked to conditional host fitness; B. agricolaris infected hosts have the highest level of co-infection and have the highest fitness in food-scarce environments. This study illuminates the phenomenon of co-infection induction across Dictyostelium associated Burkholderia species and exemplifies the contextual complexity of these associations.

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Section: Introductionmentioning

confidence: 99%

Intracellular Burkholderia Symbionts induce extracellular secondary infections; driving diverse host outcomes that vary by genotype and environment

et al. 2019

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“…Such associations are prevalent in nature, and amoebae can serve as environmental reservoirs of a wide variety of bacteria (Horn & Wagner, 2004;Nowack & Melkonian, 2010), many of which are closely-related to symbionts of insects and other organisms. Thus amoebae-bacterial interactions may be an important pathway for establishing symbioses and useful for dissecting the mechanisms of the transition to the intracellular lifestyle (Rubeniņa, Kirjušina, Bērziņš, Valciņa, & Jahundoviča, 2017;Schulz & Horn, 2015).…”

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confidence: 99%

The specificity of Burkholderia symbionts in the social amoeba farming symbiosis: Prevalence, species, genetic and phenotypic diversity

et al. 2019

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The establishment of symbioses between eukaryotic hosts and bacterial symbionts in nature is a dynamic process. The formation of such relationships depends on the life history of both partners. Bacterial symbionts of amoebae may have unique evolutionary trajectories to the symbiont lifestyle, because bacteria are typically ingested as prey. To persist after ingestion, bacteria must first survive phagocytosis. In the social amoeba Dictyostelium discoideum, certain strains of Burkholderia bacteria are able to resist amoebal digestion and maintain a persistent relationship that includes carriage throughout the amoeba's social cycle that culminates in spore formation. Some Burkholderia strains allow their host to carry other bacteria, as food. This carried food is released in new environments in a trait called farming. To better understand the diversity and prevalence of Burkholderia symbionts and the traits they impart to their amoebae hosts, we first screened 700 natural isolates of D. discoideum and found 25% infected with Burkholderia. We next used a multilocus phylogenetic analysis and identified two independent transitions by Burkholderia to the symbiotic lifestyle. Finally, we tested the ability of 38 strains of Burkholderia from D. discoideum, as well as strains isolated from other sources, for traits relevant to symbiosis in D. discoideum. Only D. discoideum native isolates belonging to the Burkholderia agricolaris, B. hayleyella, and B. bonniea species were able to form persistent symbiotic associations with D. discoideum. The Burkholderia–Dictyostelium relationship provides a promising arena for further studies of the pathway to symbiosis in a unique system.

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“…Previous work indicates that FLA function as Trojan horses for dispersal of (myco)bacteria in the environment ( 11 , 12 ), as well as training fields or biological gyms by exerting selective pressure on endosymbionts toward phenotypes that facilitate survival in human macrophages and evasion of host immune responses ( 13 , 14 ). After several days of intracellular growth in Acanthamoeba , M. avium subsp.…”

Section: Introductionmentioning

confidence: 99%

Measurable Genomic Changes in Mycobacterium avium subsp. hominissuis after Long-Term Adaptation in Acanthamoeba lenticulata and Reduced Persistence in Macrophages

et al. 2021

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Free-living amoebae are ubiquitous in aquatic environments and act as environmental reservoirs for nontuberculous mycobacteria. Mycobacterium avium subsp. hominissuis recovered from Acanthamoeba has been demonstrated to be more virulent in both human and murine models. Here, we investigate the persistence of M. avium subsp. hominissuis after short-term (2 weeks) and long-term (42 weeks) co-culture in Acanthamoeba lenticulata. We hypothesize that A. lenticulata-adapted M. avium subsp. hominissuis demonstrate phenotypic and genomic changes facilitating intracellular persistence in naïve Acanthamoeba and human macrophages. M. avium subsp. hominissuis CFU in co-culture with A. lenticulata were recorded every 2 weeks up to 60 weeks. While A. lenticulata-associated M. avium subsp. hominissuis CFU did not significantly change across 60 weeks of co-culture, longer adaptation time in amoebae reduced colony size. Isolates recovered after 2 or 42 weeks of amoebae co-culture were referred as "early-adapted" and "late-adapted" M. avium subsp. hominissuis, respectively. Whole genome sequencing was performed on amoebae-adapted isolates with pan-genome comparisons to the original M. avium subsp. hominissuis isolate. Next, amoebae-adapted isolates were assessed for their persistence in A. lenticulata, A. castellanii, and human THP-1 macrophages. Multiplex cytokine/chemokine analyses were conducted on THP-1 culture supernatants. Compared to the original isolate, counts of late-adapted M. avium subsp. hominissuis were reduced in Acanthamoeba and contrary to expectations, lower counts were also observed in THP-1 macrophages with concomitant decrease in TNFa, IL-6, and MIP-1b suggesting that host adaptation may influence the inflammatory properties of M. avium. IMPORTANCE Short-term interaction between Acanthamoeba and M. avium has been demonstrated to increase infectivity in human and murine models of infection, establishing the paradigm that amoebae "train" M. avium in the environment by selecting for phenotypes capable of enduring in human cells. We investigate this phenomenon further by determining the consequence of long-term amoebae adaptation on M. avium subsp. hominissuis persistence in host cells. We monitored genomic changes across long-term Acanthamoeba co-culture and report significant changes to the M. avium subsp. hominissuis genome in response to amoebae-adaptation and reduced colony size. Furthermore, we examined isolates co-cultured with A. lenticulata for 2 or 42 weeks and provide biological evidence that long-term co-culture in amoebae reduces M. avium persistence in human macrophages.

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Relationships between Free-Living Amoeba and their Intracellular Bacteria

Cited by 7 publications

References 66 publications

Intracellular Burkholderia Symbionts induce extracellular secondary infections; driving diverse host outcomes that vary by genotype and environment

Intracellular Burkholderia Symbionts induce extracellular secondary infections; driving diverse host outcomes that vary by genotype and environment

The specificity of Burkholderia symbionts in the social amoeba farming symbiosis: Prevalence, species, genetic and phenotypic diversity

Measurable Genomic Changes in Mycobacterium avium subsp. hominissuis after Long-Term Adaptation in Acanthamoeba lenticulata and Reduced Persistence in Macrophages

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